A chromosome-level reference genome assembly reveals extreme loss of Y-chromosomal diversity in the Saimaa ringed seal (Pusa saimensis)

Abstract

Saimaa ringed seals (Pusa saimensis) are a highly endangered freshwater pinniped species. Due to their unique evolutionary history and intense persecution over the last century, their population size and genetic diversity are low. Although mitochondrial and genome-wide variation have been extensively investigated, the paternal evolutionary history and genetic diversity of the Y chromosome remain poorly understood due to the lack of a suitable reference sequence. In this study, we take advantage of a new chromosome-level reference genome containing a curated Y chromosome and whole-genome resequencing data from 80 individuals, and characterize Y-chromosomal diversity, compare paternal and maternal lineages, and validate genomic approaches for sex determination. Read-depth analyses confirmed the accuracy of the assembled sex chromosomes, with male individuals exhibiting the expected two-fold increase in coverage across the pseudoautosomal region of chromosome X and exclusive coverage of the Y chromosome. These coverage patterns enabled reliable molecular sex determination. Phylogenetic analyses showed that both Y chromosome and mitochondrial haplotypes of the Saimaa ringed seal form distinct monophyletic clades relative to Baltic, Lake Ladoga and Arctic ringed seals, consistent with the long evolutionary isolation of the species. Similarly, the extent of genetic diversity in the Y chromosome and the mitochondrion aligned with with this long isolation history, since relative to the diversity observed across non-Saimaa ringed seals, the contemporary Saimaa population was estimated to retain only 5% of mitochondrial diversity and approximately 1% of Y-chromosomal diversity. All together, we show that chromosome-scale reference genome assemblies that include complete sex chromosomes provide a valuable resource for conservation genomics, studies of sex-specific population history, and comparative investigations of Y chromosome evolution across pinnipeds and other mammal species.